Biosystems design by directed evolution
Abstract
Through iterative rounds of genetic diversification and screening or selection, directed evolution has been widely used to engineer relatively simple biosystems such as nucleic acids and proteins with desired functions. In addition, directed evolution has played an important role in engineering more complex biosystems such as pathways and genomes. Since 2013, directed evolution has been further explored for biosystems design with numerous newly developed techniques that have enabled design and engineering of proteins, pathways, and genomes in a much more effective manner. In this review, we will highlight the abiotic biotransformations arisen from directed evolution and novel strategies for continuous evolution in vivo and ultrahigh-throughput screening. We will also discuss the future challenges and opportunities of applying directed evolution for biosystems design.
- Authors:
-
- Univ. of Illinois, Urbana-Champaign, IL (United States)
- Univ. of Illinois, Urbana-Champaign, IL (United States); Jiangnan Univ., Wuxi (China)
- Publication Date:
- Research Org.:
- Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1542919
- Alternate Identifier(s):
- OSTI ID: 1542484
- Grant/Contract Number:
- SC0018420; DE‐SC0018260; DE‐SC0018420
- Resource Type:
- Accepted Manuscript
- Journal Name:
- AIChE Journal
- Additional Journal Information:
- Journal Volume: 66; Journal Issue: 3; Journal ID: ISSN 0001-1541
- Publisher:
- American Institute of Chemical Engineers
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; directed evolution, genome engineering, pathway engineering, protein engineering, synthetic biology
Citation Formats
Wang, Yajie, Yu, Xiaowei, and Zhao, Huimin. Biosystems design by directed evolution. United States: N. p., 2019.
Web. doi:10.1002/aic.16716.
Wang, Yajie, Yu, Xiaowei, & Zhao, Huimin. Biosystems design by directed evolution. United States. https://doi.org/10.1002/aic.16716
Wang, Yajie, Yu, Xiaowei, and Zhao, Huimin. Fri .
"Biosystems design by directed evolution". United States. https://doi.org/10.1002/aic.16716. https://www.osti.gov/servlets/purl/1542919.
@article{osti_1542919,
title = {Biosystems design by directed evolution},
author = {Wang, Yajie and Yu, Xiaowei and Zhao, Huimin},
abstractNote = {Through iterative rounds of genetic diversification and screening or selection, directed evolution has been widely used to engineer relatively simple biosystems such as nucleic acids and proteins with desired functions. In addition, directed evolution has played an important role in engineering more complex biosystems such as pathways and genomes. Since 2013, directed evolution has been further explored for biosystems design with numerous newly developed techniques that have enabled design and engineering of proteins, pathways, and genomes in a much more effective manner. In this review, we will highlight the abiotic biotransformations arisen from directed evolution and novel strategies for continuous evolution in vivo and ultrahigh-throughput screening. We will also discuss the future challenges and opportunities of applying directed evolution for biosystems design.},
doi = {10.1002/aic.16716},
journal = {AIChE Journal},
number = 3,
volume = 66,
place = {United States},
year = {2019},
month = {7}
}
Web of Science
Figures / Tables:

Works referenced in this record:
Improved Cyclopropanation Activity of Histidine-Ligated Cytochrome P450 Enables the Enantioselective Formal Synthesis of Levomilnacipran
journal, May 2014
- Wang, Z. Jane; Renata, Hans; Peck, Nicole E.
- Angewandte Chemie International Edition, Vol. 53, Issue 26
De novo design of potent and selective mimics of IL-2 and IL-15
journal, January 2019
- Silva, Daniel-Adriano; Yu, Shawn; Ulge, Umut Y.
- Nature, Vol. 565, Issue 7738
Automated multiplex genome-scale engineering in yeast
journal, May 2017
- Si, Tong; Chao, Ran; Min, Yuhao
- Nature Communications, Vol. 8, Issue 1
Enzymatic assembly of carbon–carbon bonds via iron-catalysed sp3 C–H functionalization
journal, December 2018
- Zhang, Ruijie K.; Chen, Kai; Huang, Xiongyi
- Nature, Vol. 565, Issue 7737
The coming of age of de novo protein design
journal, September 2016
- Huang, Po-Ssu; Boyken, Scott E.; Baker, David
- Nature, Vol. 537, Issue 7620
Systems Metabolic Engineering Strategies: Integrating Systems and Synthetic Biology with Metabolic Engineering
journal, August 2019
- Choi, Kyeong Rok; Jang, Woo Dae; Yang, Dongsoo
- Trends in Biotechnology, Vol. 37, Issue 8
Engineering a dirhodium artificial metalloenzyme for selective olefin cyclopropanation
journal, July 2015
- Srivastava, Poonam; Yang, Hao; Ellis-Guardiola, Ken
- Nature Communications, Vol. 6, Issue 1
Optimization of Enzyme Mechanism along the Evolutionary Trajectory of a Computationally Designed (Retro-)Aldolase
journal, August 2017
- Zeymer, Cathleen; Zschoche, Reinhard; Hilvert, Donald
- Journal of the American Chemical Society, Vol. 139, Issue 36
Directed evolution: Past, present, and future
journal, January 2013
- Cobb, Ryan E.; Chao, Ran; Zhao, Huimin
- AIChE Journal, Vol. 59, Issue 5
Biosynthesis of plant-derived ginsenoside Rh2 in yeast via repurposing a key promiscuous microbial enzyme
journal, July 2017
- Zhuang, Yu; Yang, Guang-Yu; Chen, Xiaohui
- Metabolic Engineering, Vol. 42
Recent advances in metabolic engineering of Saccharomyces cerevisiae: New tools and their applications
journal, November 2018
- Lian, Jiazhang; Mishra, Shekhar; Zhao, Huimin
- Metabolic Engineering, Vol. 50
Evolution-guided optimization of biosynthetic pathways
journal, December 2014
- Raman, Srivatsan; Rogers, Jameson K.; Taylor, Noah D.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 50, p. 17803-17808
Continuous evolution of Bacillus thuringiensis toxins overcomes insect resistance
journal, April 2016
- Badran, Ahmed H.; Guzov, Victor M.; Huai, Qing
- Nature, Vol. 533, Issue 7601
Adaptive evolution of genomically recoded Escherichia coli
journal, February 2018
- Wannier, Timothy M.; Kunjapur, Aditya M.; Rice, Daniel P.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 12
Methods and Applications of CRISPR-Mediated Base Editing in Eukaryotic Genomes
journal, October 2017
- Hess, Gaelen T.; Tycko, Josh; Yao, David
- Molecular Cell, Vol. 68, Issue 1
Genetic Optimization of Metalloenzymes: Enhancing Enzymes for Non-Natural Reactions
journal, March 2016
- Hyster, Todd K.; Ward, Thomas R.
- Angewandte Chemie International Edition, Vol. 55, Issue 26
How adaptive evolution reshapes metabolism to improve fitness: recent advances and future outlook
journal, December 2018
- Long, Christopher P.; Antoniewicz, Maciek R.
- Current Opinion in Chemical Engineering, Vol. 22
A serine-substituted P450 catalyzes highly efficient carbene transfer to olefins in vivo
journal, June 2013
- Coelho, Pedro S.; Wang, Z. Jane; Ener, Maraia E.
- Nature Chemical Biology, Vol. 9, Issue 8
Evolution of a designed retro-aldolase leads to complete active site remodeling
journal, June 2013
- Giger, Lars; Caner, Sami; Obexer, Richard
- Nature Chemical Biology, Vol. 9, Issue 8
Continuous directed evolution of proteins with improved soluble expression
journal, August 2018
- Wang, Tina; Badran, Ahmed H.; Huang, Tony P.
- Nature Chemical Biology, Vol. 14, Issue 10
Beyond Iron: Iridium-Containing P450 Enzymes for Selective Cyclopropanations of Structurally Diverse Alkenes
journal, April 2017
- Key, Hanna M.; Dydio, Paweł; Liu, Zhennan
- ACS Central Science, Vol. 3, Issue 4
Computational tools for the evaluation of laboratory-engineered biocatalysts
journal, January 2017
- Romero-Rivera, Adrian; Garcia-Borràs, Marc; Osuna, Sílvia
- Chemical Communications, Vol. 53, Issue 2
Enantioselective Enzyme-Catalyzed Aziridination Enabled by Active-Site Evolution of a Cytochrome P450
journal, April 2015
- Farwell, Christopher C.; Zhang, Ruijie K.; McIntosh, John A.
- ACS Central Science, Vol. 1, Issue 2
Cytochrome P450-catalyzed insertion of carbenoids into N–H bonds
journal, January 2014
- Wang, Z. Jane; Peck, Nicole E.; Renata, Hans
- Chem. Sci., Vol. 5, Issue 2
An artificial metalloenzyme with the kinetics of native enzymes
journal, October 2016
- Dydio, P.; Key, H. M.; Nazarenko, A.
- Science, Vol. 354, Issue 6308
Adaptive laboratory evolution of a genome-reduced Escherichia coli
journal, February 2019
- Choe, Donghui; Lee, Jun Hyoung; Yoo, Minseob
- Nature Communications, Vol. 10, Issue 1
Genome-scale engineering of Saccharomyces cerevisiae with single-nucleotide precision
journal, May 2018
- Bao, Zehua; HamediRad, Mohammad; Xue, Pu
- Nature Biotechnology, Vol. 36, Issue 6
CRISPR-Mediated Base Editing Enables Efficient Disruption of Eukaryotic Genes through Induction of STOP Codons
journal, September 2017
- Billon, Pierre; Bryant, Eric E.; Joseph, Sarah A.
- Molecular Cell, Vol. 67, Issue 6
Rapid profiling of a microbial genome using mixtures of barcoded oligonucleotides
journal, July 2010
- Warner, Joseph R.; Reeder, Philippa J.; Karimpour-Fard, Anis
- Nature Biotechnology, Vol. 28, Issue 8, p. 856-862
CRISPR-STOP: gene silencing through base-editing-induced nonsense mutations
journal, June 2017
- Kuscu, Cem; Parlak, Mahmut; Tufan, Turan
- Nature Methods, Vol. 14, Issue 7
Recoded organisms engineered to depend on synthetic amino acids
journal, January 2015
- Rovner, Alexis J.; Haimovich, Adrian D.; Katz, Spencer R.
- Nature, Vol. 518, Issue 7537
A general strategy for expanding polymerase function by droplet microfluidics
journal, April 2016
- Larsen, Andrew C.; Dunn, Matthew R.; Hatch, Andrew
- Nature Communications, Vol. 7, Issue 1
An orthogonal DNA replication system in yeast
journal, February 2014
- Ravikumar, Arjun; Arrieta, Adrian; Liu, Chang C.
- Nature Chemical Biology, Vol. 10, Issue 3
Genome-wide mapping of mutations at single-nucleotide resolution for protein, metabolic and genome engineering
journal, December 2016
- Garst, Andrew D.; Bassalo, Marcelo C.; Pines, Gur
- Nature Biotechnology, Vol. 35, Issue 1, p. 48-55
Biocatalysis in Organic Chemistry and Biotechnology: Past, Present, and Future
journal, August 2013
- Reetz, Manfred T.
- Journal of the American Chemical Society, Vol. 135, Issue 34
Engineering Cellular Metabolism
journal, March 2016
- Nielsen, Jens; Keasling, Jay D.
- Cell, Vol. 164, Issue 6
Design by Directed Evolution
journal, March 1998
- Arnold, Frances H.
- Accounts of Chemical Research, Vol. 31, Issue 3
A system for the continuous directed evolution of proteases rapidly reveals drug-resistance mutations
journal, October 2014
- Dickinson, Bryan C.; Packer, Michael S.; Badran, Ahmed H.
- Nature Communications, Vol. 5, Issue 1
Computational Enzyme Design
journal, March 2013
- Kiss, Gert; Çelebi-Ölçüm, Nihan; Moretti, Rocco
- Angewandte Chemie International Edition, Vol. 52, Issue 22
Enzyme-Controlled Nitrogen-Atom Transfer Enables Regiodivergent C–H Amination
journal, October 2014
- Hyster, Todd K.; Farwell, Christopher C.; Buller, Andrew R.
- Journal of the American Chemical Society, Vol. 136, Issue 44
Design and evolution of enzymes for non-natural chemistry
journal, October 2017
- Hammer, Stephan C.; Knight, Anders M.; Arnold, Frances H.
- Current Opinion in Green and Sustainable Chemistry, Vol. 7
Multiplexed tracking of combinatorial genomic mutations in engineered cell populations
journal, March 2015
- Zeitoun, Ramsey I.; Garst, Andrew D.; Degen, George D.
- Nature Biotechnology, Vol. 33, Issue 6, p. 631-637
Scalable, Continuous Evolution of Genes at Mutation Rates above Genomic Error Thresholds
journal, December 2018
- Ravikumar, Arjun; Arzumanyan, Garri A.; Obadi, Muaeen K. A.
- Cell, Vol. 175, Issue 7
Directed evolution of artificial metalloenzymes for in vivo metathesis
journal, August 2016
- Jeschek, Markus; Reuter, Raphael; Heinisch, Tillmann
- Nature, Vol. 537, Issue 7622
Engineering microbial factories for synthesis of value-added products
journal, April 2011
- Du, Jing; Shao, Zengyi; Zhao, Huimin
- Journal of Industrial Microbiology & Biotechnology, Vol. 38, Issue 8
Evolution of enzyme catalysts caged in biomimetic gel-shell beads
journal, July 2014
- Fischlechner, Martin; Schaerli, Yolanda; Mohamed, Mark F.
- Nature Chemistry, Vol. 6, Issue 9
Abiological catalysis by artificial haem proteins containing noble metals in place of iron
journal, June 2016
- Key, Hanna M.; Dydio, Paweł; Clark, Douglas S.
- Nature, Vol. 534, Issue 7608
Experimental interrogation of the path dependence and stochasticity of protein evolution using phage-assisted continuous evolution
journal, May 2013
- Dickinson, B. C.; Leconte, A. M.; Allen, B.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 22
Harnessing mutagenic homologous recombination for targeted mutagenesis in vivo by TaGTEAM
journal, March 2013
- Finney-Manchester, Shawn P.; Maheshri, Narendra
- Nucleic Acids Research, Vol. 41, Issue 9
Direct Mutagenesis of Thousands of Genomic Targets Using Microarray-Derived Oligonucleotides
journal, June 2014
- Bonde, Mads T.; Kosuri, Sriram; Genee, Hans J.
- ACS Synthetic Biology, Vol. 4, Issue 1
Improving and repurposing biocatalysts via directed evolution
journal, April 2015
- Denard, Carl A.; Ren, Hengqian; Zhao, Huimin
- Current Opinion in Chemical Biology, Vol. 25
Directed Evolution of Protein Catalysts
journal, June 2018
- Zeymer, Cathleen; Hilvert, Donald
- Annual Review of Biochemistry, Vol. 87, Issue 1
De novo biosynthesis of Gastrodin in Escherichia coli
journal, May 2016
- Bai, Yanfen; Yin, Hua; Bi, Huiping
- Metabolic Engineering, Vol. 35
Rational design of a synthetic Entner–Doudoroff pathway for improved and controllable NADPH regeneration
journal, May 2015
- Ng, Chiam Yu; Farasat, Iman; Maranas, Costas D.
- Metabolic Engineering, Vol. 29
Ultrahigh-throughput–directed enzyme evolution by absorbance-activated droplet sorting (AADS)
journal, November 2016
- Gielen, Fabrice; Hours, Raphaelle; Emond, Stephane
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 47
Precise Editing at DNA Replication Forks Enables Multiplex Genome Engineering in Eukaryotes
journal, November 2017
- Barbieri, Edward M.; Muir, Paul; Akhuetie-Oni, Benjamin O.
- Cell, Vol. 171, Issue 6
Olefin Cyclopropanation via Carbene Transfer Catalyzed by Engineered Cytochrome P450 Enzymes
journal, December 2012
- Coelho, P. S.; Brustad, E. M.; Kannan, A.
- Science, Vol. 339, Issue 6117
Ultrahigh-throughput discovery of promiscuous enzymes by picodroplet functional metagenomics
journal, December 2015
- Colin, Pierre-Yves; Kintses, Balint; Gielen, Fabrice
- Nature Communications, Vol. 6, Issue 1
High-throughput analysis and protein engineering using microcapillary arrays
journal, December 2015
- Chen, Bob; Lim, Sungwon; Kannan, Arvind
- Nature Chemical Biology, Vol. 12, Issue 2
Enantioselective Intramolecular CH Amination Catalyzed by Engineered Cytochrome P450 Enzymes In Vitro and In Vivo
journal, July 2013
- McIntosh, John A.; Coelho, Pedro S.; Farwell, Christopher C.
- Angewandte Chemie International Edition, Vol. 52, Issue 35
A system for the continuous directed evolution of biomolecules
journal, April 2011
- Esvelt, Kevin M.; Carlson, Jacob C.; Liu, David R.
- Nature, Vol. 472, Issue 7344
Combinatorial metabolic engineering using an orthogonal tri-functional CRISPR system
journal, November 2017
- Lian, Jiazhang; HamediRad, Mohammad; Hu, Sumeng
- Nature Communications, Vol. 8, Issue 1
Exploiting and engineering hemoproteins for abiological carbene and nitrene transfer reactions
journal, October 2017
- Brandenberg, Oliver F.; Fasan, Rudi; Arnold, Frances H.
- Current Opinion in Biotechnology, Vol. 47
De novo enzymes by computational design
journal, April 2013
- Kries, Hajo; Blomberg, Rebecca; Hilvert, Donald
- Current Opinion in Chemical Biology, Vol. 17, Issue 2
Directed Evolution of Single Proteins, Metabolic Pathways, and Viruses
journal, November 2001
- Schmidt-Dannert, Claudia
- Biochemistry, Vol. 40, Issue 44
Enzymatic construction of highly strained carbocycles
journal, April 2018
- Chen, Kai; Huang, Xiongyi; Kan, S. B. Jennifer
- Science, Vol. 360, Issue 6384
Exploring sequence space in search of functional enzymes using microfluidic droplets
journal, April 2017
- Mair, Philip; Gielen, Fabrice; Hollfelder, Florian
- Current Opinion in Chemical Biology, Vol. 37
RNAi-Assisted Genome Evolution in Saccharomyces cerevisiae for Complex Phenotype Engineering
journal, May 2014
- Si, Tong; Luo, Yunzi; Bao, Zehua
- ACS Synthetic Biology, Vol. 4, Issue 3
The Molecular Diversity of Adaptive Convergence
journal, January 2012
- Tenaillon, O.; Rodriguez-Verdugo, A.; Gaut, R. L.
- Science, Vol. 335, Issue 6067, p. 457-461
Genetically programmed chiral organoborane synthesis
journal, November 2017
- Kan, S. B. Jennifer; Huang, Xiongyi; Gumulya, Yosephine
- Nature, Vol. 552, Issue 7683
Directed evolution of a cellobiose utilization pathway in Saccharomyces cerevisiae by simultaneously engineering multiple proteins
journal, January 2013
- Eriksen, Dawn T.; Hsieh, Pei Chiun; Lynn, Patrick
- Microbial Cell Factories, Vol. 12, Issue 1
CRISPR-guided DNA polymerases enable diversification of all nucleotides in a tunable window
journal, August 2018
- Halperin, Shakked O.; Tou, Connor J.; Wong, Eric B.
- Nature, Vol. 560, Issue 7717
Expanding the Enzyme Universe: Accessing Non-Natural Reactions by Mechanism-Guided Directed Evolution
journal, February 2015
- Renata, Hans; Wang, Z. Jane; Arnold, Frances H.
- Angewandte Chemie International Edition, Vol. 54, Issue 11
Evolved Cas9 variants with broad PAM compatibility and high DNA specificity
journal, February 2018
- Hu, Johnny H.; Miller, Shannon M.; Geurts, Maarten H.
- Nature, Vol. 556, Issue 7699
Anti-Markovnikov alkene oxidation by metal-oxo–mediated enzyme catalysis
journal, October 2017
- Hammer, Stephan C.; Kubik, Grzegorz; Watkins, Ella
- Science, Vol. 358, Issue 6360
ALEdb 1.0: a database of mutations from adaptive laboratory evolution experimentation
journal, October 2018
- Phaneuf, Patrick V.; Gosting, Dennis; Palsson, Bernhard O.
- Nucleic Acids Research, Vol. 47, Issue D1
Artificial Metalloenzymes: Reaction Scope and Optimization Strategies
journal, May 2017
- Schwizer, Fabian; Okamoto, Yasunori; Heinisch, Tillmann
- Chemical Reviews, Vol. 118, Issue 1
In vivo continuous evolution of genes and pathways in yeast
journal, October 2016
- Crook, Nathan; Abatemarco, Joseph; Sun, Jie
- Nature Communications, Vol. 7, Issue 1
Emergence of a catalytic tetrad during evolution of a highly active artificial aldolase
journal, August 2016
- Obexer, Richard; Godina, Alexei; Garrabou, Xavier
- Nature Chemistry, Vol. 9, Issue 1
Chemoselective, Enzymatic C–H Bond Amination Catalyzed by a Cytochrome P450 Containing an Ir(Me)-PIX Cofactor
journal, January 2017
- Dydio, Paweł; Key, Hanna M.; Hayashi, Hiroki
- Journal of the American Chemical Society, Vol. 139, Issue 5
Directed evolution of a highly efficient cellobiose utilizing pathway in an industrial Saccharomyces cerevisiae strain : Directed Evolution of a Cellobiose Pathway
journal, June 2013
- Yuan, Yongbo; Zhao, Huimin
- Biotechnology and Bioengineering, Vol. 110, Issue 11
Yeast Oligo-Mediated Genome Engineering (YOGE)
journal, November 2013
- DiCarlo, James E.; Conley, Andrew J.; Penttilä, Merja
- ACS Synthetic Biology, Vol. 2, Issue 12
Genomically Recoded Organisms Expand Biological Functions
journal, October 2013
- Lajoie, M. J.; Rovner, A. J.; Goodman, D. B.
- Science, Vol. 342, Issue 6156, p. 357-360
Improved Cyclopropanation Activity of Histidine-Ligated Cytochrome P450 Enables the Enantioselective Formal Synthesis of Levomilnacipran
journal, May 2014
- Wang, Z. Jane; Renata, Hans; Peck, Nicole E.
- Angewandte Chemie, Vol. 126, Issue 26
Enantioselective Intramolecular CH Amination Catalyzed by Engineered Cytochrome P450 Enzymes In Vitro and In Vivo
journal, July 2013
- McIntosh, John A.; Coelho, Pedro S.; Farwell, Christopher C.
- Angewandte Chemie, Vol. 125, Issue 35
WebLogo: A Sequence Logo Generator
journal, May 2004
- Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc
- Genome Research, Vol. 14, Issue 6, p. 1188-1190
A serine-substituted P450 catalyzes highly efficient carbene transfer to olefins in vivo
text, January 2013
- S., Coelho, Pedro; H., Arnold, Frances; E., Ener, Maraia
- The University of North Carolina at Chapel Hill University Libraries
Exploring sequence space in search of functional enzymes using microfluidic droplets
text, January 2017
- Mair, P.; Gielen, F.; Hollfelder, Florian
- Apollo - University of Cambridge Repository
Optimization of Enzyme Mechanism along the Evolutionary Trajectory of a Computationally Designed (Retro-)Aldolase
text, January 2017
- Zeymer, Cathleen; Zschoche, Reinhard; Hilvert, Donald
- ETH Zurich
Evolution of enzyme catalysts caged in biomimetic gel-shell beads
text, January 2014
- Fischlechner, Martin; Schaerli, Yolanda; Mohamed, Mark F.
- Nature Publishing Group
Emergence of a catalytic tetrad during evolution of a highly active artificial aldolase
text, January 2017
- Obexer, Richard; Godina, Alexei; Garrabou, Xavier
- Nature Publishing Group
De novo design of potent and selective mimics of IL-2 and IL-15.
text, January 2019
- Silva, Daniel-Adriano; Yu, Shawn; Ulge, Umut Y.
- Apollo - University of Cambridge Repository
Figures / Tables found in this record: